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179Intracranial Stroke-related B-mode Pathology
Valdueza et al., Neurosonology and Neuroimaging of Stroke: A Comprehensive Reference, Second Edition (ISBN 978-3-13-141872-2), copyright © 2017 Thieme Medical Publishers
All rights reserved. Usage subject to terms and conditions of license.
Fig. A5.181 TCS- MRI f usion imag ing ( MyLa b Twice, E saote ) of a patient with hydrocephalus, thalamic insonation plane. Top left: TCBS
with enlarged third ventricle of 15 mm (double-headed arrow).
Top ri ght : Correspondingly matched MR T1-weighted postcontrast
image. Bottom: Overlap projection of TCBS and MRI.
The above TCBS-derived data on normal individuals are
well within the range of the available data from the radiologic literature. Early CCT analysis of 100 healthy individuals
demonstrated a mean diameter of 3.2 mm in the 17–40 year
age group and 5 mm in the 41–86 year age group (Gyldensted 1977). MRI-derived third ventricle diameters in individuals aged 20–50 were reported to be 3.8 ± 0.9 mm for
females and 4.1 ± 0.9 mm in males (Karakaş et al 2011).
Hydrocephalus
Intracranial mass hemorrhage or subarachnoid hemorrhage may lead to impaired cerebrospinal fl uid (CSF)
drainage and subsequent obstructive hydrocephalus
which may require therapeutic intervention with external ventricular drainage. Despite the fact that widening
of the third and lateral ventricles can be visualized by
TCBS the approach can also be used for direct treatment
decisions, e.g., deciding when to remove external ventricular drainage (Fig. A5.181, Fig. A5.182, Fig. A5.183).
Kiphuth and coworkers reported a cut-off value of
5.5 mm increase of ventricular width after external ventricular drainage clamping (Kiphuth et al 2011). Increases below this value were considered safe by the authors
for drainage removal.
Papilledema and Optic Nerve Sheath Diameter
Papilledema and an increase of the optic nerve sheath
diameter (ONSD) are indirect signs of raised intracranial pressure (ICP) that may be caused by a large cerebral
infarction or intracranial hemorrhage. As the optic nerve
sheath is an extension of the subarachnoid space and as
is by its structure expandable, an ICP increase may lead
to its enlargement which is, like the optic papilla, accessible to ultrasound (Helmke and Hansen 1996a, 1996b).
Assessments are usually made using a conventional linear probe with insonation frequencies ranging from 7 to
15 MHz. Care has to be taken that the insonation pow-
Fig. A5.182 TCS- MRI fus ion ima ging (MyLab Twice, E saot e) of
a patient with hydrocephalus, cella media insonation plane. Top
left: TCBS with enlarged lateral ventricle of 28 mm (double-headed arrow). Top r igh t: Correspondingly matched MR T1-weighted
postcontrast image, Bottom: Overlap projection of TCBS and MRI.
Fig. A5.183 TCS-MRI fusion imaging (MyLab Twice, Esaote) of a
patient with hydrocephalus, anterior coronal insonation plane. Top
left: TCBS with enlarged lateral ventricle of 24 mm (double-headed arrow). To p right : Correspondingly matched MR T1-weighted
postcontrast image. Bottom: Overlap projection of TCBS and MRI.
er remains below a mechanical index (MI) of 0.26 at any
time to protect the insonated eye from any potential ultrasound-related side eff ects.
Papilledema appears on ultrasound as a domeshaped prominence of the optic disk, its extent measurable (in mm) as distance from the level of the retina
(Fig. A5.184A,B). A disc height greater than 0.6 mm predicts the presence of fundoscopic optic disc edema with
82% sensitivity of and 76% specifi city. A threshold value
of 1.0 mm was shown to yield 73% sensitivity and 100%
specifi city (Teismann et al 2013a). In diff erential diagno-
sis diff erentiation from optic disc drusen by ultrasound
is not diffi cult as the latter present calcium deposits that
are detectable as hyperechoic lesions on the ultrasound
image (Fig. A5.184C).
Ultrasound assessment of ONSD has been described
as a useful tool in several studies of patients with raised
180 5 Vascular Pathology
Valdueza et al., Neurosonology and Neuroimaging of Stroke: A Comprehensive Reference, Second Edition (ISBN 978-3-13-141872-2), copyright © 2017 Thieme Medical Publishers
All rights reserved. Usage subject to terms and conditions of license.
A
B
Fig. A5.184 Tra ns or bi ta l ins on at io n of th e ey e bul b, l in ear t ra ns duc er, 15 MHz, MI 0.20. (A) Dome-shaped optic disc swelling, prominence 1.1 mm. For estimation of the retinal level a circular measure
(dotted line) can be applied. (B) Optic disc swelling and increased
optic nerve sheath diameter (ONSD) 6.5 mm. The double-headed
arrow indicates the required 3 mm distance to the retinal level. The
horizontal line indicates the ONSD width, delineated by the outer
borders of the hyperechoic optic nerve sheath which surrounds the
hypoechoic optic nerve. (C) Optic disk drusen; note the calcifi ed as-
pect of the papillary prominence (arrow). (D) No optic disk swelling is
present but raised ONSD 6.7 mm indicating acute or subacute raised
intracranial pressure, not yet resulting in papilledema.
C
D
8.82 cm7.69 cm
MLS=
(A-B)/2
Fig. A5.185 Mild midline shift at the level of the third ventricle in
a patient with a large left-sided arachnoid cyst. Top lef t a nd righ t:
TCBS me asure ment s of th e distance fr om probe to the middle o f the
third ventricle contra- and ipsilateral to the cyst. Right side 7.69 cm,
left side 8.82 cm. MLS calculation: (8.82 − 7.69)/2= 0.57 cm.
ICP (Geeraerts et al 2008, Soldatos et al 2008) as well as in
healthy controls (Bäuerle et al 2012, Steinborn et al 2015).
Ultrasound-derived values are reported to be in good correlation with MR-derived data. Intra- and interobserver
reliability is high. The ONSD is assessed 3 mm posterior to
the optic disk (Fig. A5.184C,D; see also Video
A2.20).
Normal values in healthy volunteers show a mean diameter of 5.4 ± 0.6 mm (range 4.3–7.6 mm) (Bäuerle et al 2012).
Midline and Midline Shift
As identifi cation of the third ventricle is simple and reli-
able, the search for a potential midline shift at this level
can be done easily. The distance from probe to midline—
defi ned as the middle of the third ventricle—is measured
through the transtemporal bone window from ipsilateral and contralateral. The resulting measures A and B are
then used for midline shift calculation; an example is
given in Fig. A5.185:
Midline shift (MLS) = (A − B)/2
The applicability, validity, and relevance of transcranial MLS measurements have been assessed in several
studies. The fi rst analyses were reported in a group of
10 healthy volunteers who demonstrated a mean dislocation of 0.2 ± 0.3 mm (Seidel et al 1996). In the same study,
results from 18 stroke patients were correlated with CT
measurements, yielding a correlation coeffi cient of 0.87.
A second study prospectively analyzed 61 patients with
supratentorial ischemia or hemorrhage in comparison
with cranial CT in a time window of 12 hours, confi rming
the above fi ndings with a signifi cant correlation coeffi -
cient of 0.93 (Stolz et al 1999d).
Subsequently published studies were looking for the
clinical importance of the MLS analysis in acute stroke patients (Gerriets et al 1999, 2001). Serial monitoring of MLS
at 8, 16, 24, 32, and 40 hours revealed a prognostic value
visible as early as 16 hours after stroke onset. A positive
predictive value of 1 for a fatal outcome at 16 hours was
found with a MLS of >2.5 mm (negative predictive value
0.96). At 24 hours a MLS of >3.5 mm predicted a fatal outcome with a sensitivity and specifi city of 100%, unless the
patient was treated by a hemicraniectomy (Tab le A5.3 ).
However, hemicraniectomy might be required even
if the above MLS values are not reached, e.g., because
of a dramatic clinical deterioration caused by an ultrasound-inaccessible herniation pattern, especially in
temporal space-occupying masses. More recently, MLS
analysis was reported as a useful bedside tool for the
assessment of supratentorial intracranial hemorrhage
(Tang et al 2005). As in patients with ischemia, MLS is
suitable for the prediction of the clinical outcome. It was
found that in these patients, monitored on a daily basis
for 14 days, a MLS ≥12 mm was indicative for mortality
with 69% sensitivity, 100% specifi city, and positive and
negative predictive values of 100% and 74%, respectively
(Kiphuth et al 2012).
Intracranial Hemorrhage
Parenchymal Hemorrhage
Intraparenchymal hemorrhages (IPH) can be seen in
B-mode images (Fig. A5.186 and Fig. A5.187). In 1993
Seidel and coworkers published a study of 23 consecutive
patients with IPH of diff erent origin. They could correct-
ly identify the hemorrhage in 18 of these patients (78%)
Table A5.3 Sensitivity, specifi city, and predictive values for a midline shift (MLS) of 1.25, 2.5, 3.5, 4.0, and 5.0 mm, indicating fatal outcome
Valdueza et al., Neurosonology and Neuroimaging of Stroke: A Comprehensive Reference, Second Edition (ISBN 978-3-13-141872-2), copyright © 2017 Thieme Medical Publishers
All rights reserved. Usage subject to terms and conditions of license.
8, 16, 24, 32, and 40 hours after stroke. Probability values indicate statistical diff erence of MLS between patients who died and those who
survived. (Data from Gerriets et al 2001).
TCCS MLS Time (h) Sensitivity Specifi city PPV NPV n P
>1.25 mm 8 ± 3 0.56 0.83 0.56 0.83 33 NS
>2.5 mm 16 ± 3 0.83 1.00 1.00 0.96 29 <0.001
>3.5 mm
>4.0 mm 32 ± 3 1.00 1.00 1.00 1.00 29 <0.001
>5.0 mm 40 ± 3 1.00 1.00 1.00 1.00 23 <0.001
MLS, midline shift; NPV, negative predictive value; PPV, positive predictive value; TCCS, transcranial color-coded duplex sonography.
24 ± 3 1.00 1.00 1.00 1.00 26 <0.001
181Intracranial Stroke-related B-mode Pathology
Fig. A5.186 TCS- MRI fu sion i maging (MyLab Twice, Es aote) . US
and CT in axial planes. Top: Example of a patient with a large lobar
hemorrhage (arrows). Bottom: Example of a patient with a large
basal ganglia hemorrhage (arrows). Left: B-mode US image. Right:
CT image, exactly matched with the calculated 3D dataset of the
fusion imaging system.
while 3 had to be excluded because of an insuffi cient
transtemporal bone window. However, one small lobar
hemorrhage could not be identifi ed and one extensive
basal ganglia hematoma was misinterpreted as lobar
hematoma. Follow-up analysis over 3 weeks posthemorrhage revealed three typical phases of hematoma appearance (Seidel et al 1993):
• Phase 1 (days 1–5): Hyperechoic phase.
• Phase 2 (days 6–10): Gradual decline of echogenicity in
the hematoma center.
• Phase 3 (days 11–21): Central hypoechogenicity and
small echogenic margin.
The approach was subsequently applied by other groups
who studied 46 and of 39 patients with IPH, yielding detection rates in which ICH was missed in 17% and 13% of cases,
respectively (Kukulska-Pawluczuk et al 2012, Pérez et al
2009). However, the correlation of the remaining detectable
cases with the concomitant CCT in both studies was good.
Interestingly, not only primary but also secondary
intracranial hemorrhagic transformation after ischemic
stroke can be assessed by transcranial B-mode imaging
(Fig. A5.188). In a series of 11 patients with ischemic
MCA infarction who developed secondary hemorrhagic transformation, ultrasound assessment yielded one
Fig. A5.187 TCS- MRI fusi on im aging (MyL ab Twice, Esaot e). US and
CT in axial planes. Top: Example of a patient with a small thalamic
hemorrhage (arrows). Bottom: Example of a patient with a small
cerebellar hemorrhage (arrows). Left: B-mode US image. Right:
CT image, exactly matched with the calculated three-dimensional
dataset of the fusion imaging system.
Fig. A5.188 TCS- MRI fu sion i maging (MyLab Twice, Es aote) . US
and CT in axial planes. Top: Example of a patient with posterior stri-
atal infarction and secondary hemorrhagic imbibition 3 days after
stroke onset (arrows). Left: B-mode US image. Right: CT image,
exactly matched with the calculated 3D dataset of the fusion imaging system. Bottom: Same image set demonstrating manual lesion
assessment with good measurement correspondence.
182 5 Vascular Pathology
Valdueza et al., Neurosonology and Neuroimaging of Stroke: A Comprehensive Reference, Second Edition (ISBN 978-3-13-141872-2), copyright © 2017 Thieme Medical Publishers
All rights reserved. Usage subject to terms and conditions of license.
Fig. A5.189 TCS -MRI fu sion imagin g (M yLab Twice, Esaote ). Exam ple of a patient with an acute subdural hematoma (small arrows)
with homogenous hyperechoic appearance caused by spontaneous
intracranial hypotension. Top: Axial plane imaging. Bottom: Coronal plane imaging. Left: B-mode US image. Right: CT image, exactly matched with the calculated 3D dataset of the fusion imaging
system. Note the exact matching of US and CT imaging planes with
US delineation of the anterior horn of the lateral ventricle (short
arrow) and the petrosal bone (long arrow).
false- positive and one false-negative fi nding, corre-
sponding to a calculated sensitivity and specifi city of
91% and 95%, respectively (Seidel et al 2005). The same
group published another consecutive series of 20 stroke
patients with and without systemic thrombolysis. The
former showed hemorrhagic transformation in 62.5%,
the latter in 33% of cases. Detection rates, compared
with CCT were similar to the previous study (90.0% sensitivity, 97.4% specifi city).
In one prospective study of 151 patients with acute
hemiparesis of whom 60 had an IPH, TCBS diff erentiat-
ed correctly between ischemia and hemorrhage in 95%
of the assessable patients (Mäurer et al 1998). However,
three IPH patients remained undetected and another four
were assessed as false positives.
Recently, ultrasound fusion imaging—a new insonation approach, permitting simultaneous analysis of live
ultrasound images with digitally matched CT or MR
images—has become available (for further reading, see
Chapter 1, “Ultrasound Fusion Imaging”). Early reports
describe its application in patients with diff erent in-
tracranial pathologies (Schreiber et al 2014a, 2014c).
The technique has also been used to study patients
with intracranial hemorrhages. In a small case control
study, we analyzed 21 patients with acute intracranial
mass hemorrhages of which 17 (81%) could successfully be identifi ed with TCBS (Schreiber et al 2014b).
Subgroup analysis showed better detection rates for
basal ganglia location (91%), compared with cortical
location (67%).
Subdural and Epidural Hematoma
Subdural and epidural hematoma may also be detected
using TCBS (Fig. A5.189 and Fig. A5.190). The fi rst re-
port on subdural hematoma detection was published
Fig. A5.190 TCS -MRI fu sion im agin g ( MyLa b Twice, E saote ):
E x a m p l e o f a p a t i e n t w i t h a c h r o n i c s u b d u r a l h e m a t o m a ( s m a l l
a r r o w s ) . U S a n d C T i n a x i a l p l a n e . N o t e t h e i s o e c h o i c a s p e c t o f t h e
hematoma and hyperechoic dural border. Arrow: corresponding
delineation of the anterior horn of the lateral ventricle. Bottom:
Orientation of insonation plane in relation to the three spatial
planes, derived from the 3D dataset of the fusion imaging system.
in 1991, describing sonographic hematoma appearance
and secondary eff ects on midline, ventricles, and brain
parenchyma in 14 SDH patients (Lam and Cruz 1991).
In another small group of patients subdural hematoma
was correctly detected in 18 of 19 patients (Woydt et al
1996). The largest study so far analyzed 25 patients with
SDH in whom 22 (88%) were correctly diagnosed and 3
could not be evaluated because of a missing transtemporal bone window (Niesen et al 2006). The authors found a
homogenous hyperechoic appearance in acute SDH and
a hypoechoic appearance under the hyperechoic dural
border in patients with chronic SDH. However, applying
this evaluation approach, TCBS misdiagnosed the SDH
age in 18% of cases. Correlation analysis of TCBS and CCT
hematoma measures yielded a correlation coeffi cient of
r = 0.85. More recently, a case report of a posttraumatic SDH diagnosed in the Emergency Department while
awaiting CT scan has suggested a potential screening
application in the fi eld of emergency medicine (Blanco
and Matteoda 2015).
The diagnosis of epidural hematoma is also possible
but has so far been shown only in several single cases
(Caricato et al 2010, 2014).
In summary, TCBS can easily be used for the evaluation of intracranial pathology with space-occupying
parenchymal eff ects, CSF circulation disturbances, or
direct visual assessment of intracranial hemorrhages.
It is especially relevant whenever bedside evaluation or
frequent follow-up is required, which currently leads to
repetitive CT or MRI imaging. A change toward a more
frequent use of TCBS in these instances may be accelerated by new techniques such as ultrasound fusion
imaging which facilitates lesion detection and direct
comparison of diff erent image modalities, and allows
the precise reidentifi cation of regions of interest during
repeated investigations.
6
Valdueza et al., Neurosonology and Neuroimaging of Stroke: A Comprehensive Reference, Second Edition (ISBN 978-3-13-141872-2), copyright © 2017 Thieme Medical Publishers
All rights reserved. Usage subject to terms and conditions of license.
Angiographic Techniques in Neuroradiology
183
Choice of Imaging Techniques . . . . . . . . . . . . . . . . . . 183
Digital Subtraction Angiography (DSA) . . . . . . . . . . 183
Historical Development . . . . . . . . . . . . . . . . . . . . . . . . . 183
Technical Aspects of Diagnostic Angiography . . . . . . . 184
Technical Aspects of Mechanical Thrombectomy . . . . 185
Advantages and Disadvantages . . . . . . . . . . . . . . . . . . 185
Magnetic Resonance Angiography (MRA) . . . . . . . . 187
Historical Development . . . . . . . . . . . . . . . . . . . . . . . . . 187
Choice of Imaging Techniques
In recent years various new cross-sectional imaging techniques have evolved, which makes choosing the right angiographic technique for a given purpose more and more
complicated. As various techniques, either single or combined, may provide the clinically relevant information,
the fi nal diagnostic algorithms applied will be deter-
mined by various factors such as technical infrastructure
(scanner, workstation), access throughout the week, clinical pathways presently used, and the hospital’s size and
stroke care level (stroke unit, neurosurgery). As a result
of the ongoing technical improvements, only specialized
investigators, e.g., neuroradiologists or vascular neurologists, are now able to tailor the imaging protocol to the
specifi c clinical questions of the transferring physician as
well as to the patient’s needs.
In this chapter, the angiographic methods in clinical use—
digital subtraction angiography (DSA), MR angiography
(MRA), and CT angiography (CTA)—are presented, considering their historical development, technical aspects, and
their main advantages and disadvantages. In addition, image data postprocessing techniques such as multiplanar
reformatting (MPR), maximum intensity projection (MIP),
and volume rendering (VR) have become indispensable for
extracting and visualizing pertinent clinical information
that is not available from numerous cross-sectional images. Yet, neuroangiographic data acquisition (CTA, MRA, and
DSA) as well as postprocessing techniques (MPR, MIP, and
VR) may be misleading in various ways due to inherent pitfalls and limitations. Image artifacts may mimic high-grade
vessel stenosis where there is none, whereas inappropriate
data postprocessing may hide such stenosis. Whenever
Technical Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
Advantages and Disadvantages . . . . . . . . . . . . . . . . . . 190
Computed Tomographic Angiography (CTA) . . . . . . 191
Historical Development . . . . . . . . . . . . . . . . . . . . . . . . . 191
Technical Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192
Advantages and Disadvantages . . . . . . . . . . . . . . . . . . 192
treatment decisions are based on cross-sectional imaging,
a thorough knowledge of these limitations is of paramount
importance.
The current status of neuroimaging in regard to the
major issues of stroke, intracranial hemorrhage, vessel
wall pathology and stenoses as well as in sinus venous
thrombosis is discussed in the context of the diff erent
imaging techniques. Further angiographic aspects are focused upon within the selected case histories.
Digital Subtraction Angiography (DSA)
Historical Development
Conventional angiography is a technique that uses radiographs to visualize the lumen of blood-fi lled struc-
tures, such as the cervical and cerebral arteries. The term
angiography is derived from the Greek words angeion,
meaning “vessel,” and graphien, meaning “to write” or “to
record.” The term angiograph or, more commonly nowa-
days, angiogram, denotes the radiographic image. The use
of a radiodense intravascular contrast agent is required to
outline the vessel structures; an intravenously administered contrast medium containing nonionic iodine is now
commonly used.
Egas Moniz, a Portuguese neurologist who was one
of the most important pioneers in this fi eld, developed
cerebral angiography in 1927 as a way of using contrasted
cerebral X-ray angiograms for the assessment of various
central nervous system (CNS) diseases of neoplastic and
vascular origin (Petit-Dutaillis 1954). The fi rst cerebral
angiographies were performed in 1896 by cadaver testing,
184 6 Angiographic Techniques in Neuroradiology
Valdueza et al., Neurosonology and Neuroimaging of Stroke: A Comprehensive Reference, Second Edition (ISBN 978-3-13-141872-2), copyright © 2017 Thieme Medical Publishers
All rights reserved. Usage subject to terms and conditions of license.
AB CD
Fig. A6.1 DSA (frontal view) showing diff erent phases of an ICA angiogram: (A) early arterial, (B) late arterial, (C) capillary, and (D) venous
phase. The circulation time usually amounts to ~4 seconds.
as no contrast medium suitable for use in living patients
was available at that time. When Moniz performed his
fi rst angiograms, the carotid artery had to be opened for
access. In 1929 the German physician Werner Forssmann,
who worked at the Charité hospital in Berlin, performed
the fi rst cardiac catheterization in a self-experiment and
received the Nobel Prize in 1956 for this ground-breaking
discovery (Forssmann 1954).
The use of a small intravascular tube as well as direct
percutaneous vessel puncture, introduced by the Swedish
radiologist Sven Ivar Seldinger in 1953, are the hallmarks
of modern angiography, as no sharp and potentially
harmful introductory devices need to be left inside the
vessel lumen (Seldinger 1953).
DSA, introduced in 1980 (Meaney et al 1980), permitted serial imaging while reducing radiation exposure
and contrast medium volume as compared with conventional fi lm-screen arteriography and has since remained
the gold standard technique for invasive cerebrovascular
angiography (Fig. A6.1). Contrast-enhanced (ce) images
are subtracted from the preceding plain image, thus eliminating all unnecessary image information and improving
vessel-to-background ratio.
For neuroangiographic purposes biplane angiography
suites have become standard as the morphologic depiction of aneurysms and of arteriovenous malformations
are improved, thus reducing procedure times and contrast medium volumes.
Three-dimensional (3D) rotational angiography was
introduced in 1996 and showed potential in neurointerventional treatment planning, such as assessing aneurysm
confi guration and choosing the optimal projection view
for coiling (Anxionnat et al 2001, Sugahara et al 2002).
More recently, volumetric imaging with improved spatial resolution, decreased radiation exposure and optional CT-like brain imaging has become available by using
C-arm-mounted fl at-panel technology (Dörfl er et al 2008).
Technical Aspects of Diagnostic Angiography
Briefl y, access is achieved by puncture of the femoral ar-
tery using the Seldinger technique. After intravascular
placement of the introducer sheath, a hydrophilic guide
wire is advanced to the level of the aortic arch, followed
by a catheter. Assisted by the wire, an endhole-catheter
is then moved upwards for diagnostic angiography purposes into the internal carotid and/or vertebral arteries,
depending on the particular clinical question. If anatomic
variants or signifi cant proximal supra-aortic vessel pa-
thology are expected, an aortic arch angiogram by using
the so-called pigtail catheter may be obtained fi rst.
Although the spatial resolution of DSA with a pixel size
of ~0.3 mm (Villablanca et al 2007) is closely approximated by multislice CTA (0.35 mm) contrast-to-noise ratio
is superior for DSA, thus improving delineation of very
small vessels. In particular, primary angiitis of the CNS
tends to aff ect medium-sized and smaller vessels, making
the best possible vessel delineation of major importance.
The total amount of injected iodinated nonionic contrast medium varies according to the particular procedure, e.g., whether or not a brachiocephalic angiogram
(BCAG) is required. A maximum of ~80 mL contrast medium (300 mg I/mL) is required for a four-vessel angiogram
including BCAG.
DSA not only provides pathomorphologic information, but visualizes intracerebral hemodynamics (e.g.,
collateral blood fl ow or arteriovenous shunting) by re-
peatedly acquiring multiple images per second.
In rotational 3D DSA, also called fl at-panel vol-
ume CT, a fi xed C-arm rotates around the patient and
acquires a few hundred X-ray images, which are subsequently transformed into 3D images by software
algorithms (Gupta et al 2008, Wallace et al 2009).
C-arm–volume CT off ers fl exibility in positioning the
detector around the patient and provides advanced
fl uoroscopic capability, thus being particularly suitable
for interventional angiographic purposes. The resulting
3D images are commonly used in the morphological
assessment of aneurysms or cerebrovascular malformations (Fig. A6.2). It thus supports various diagnostic
and neurointerventional procedures, such as intracranial stenting, stent-assisted coil embolization, or arteriovenous malformation (AVM) embolization ( Dörfl er
et al 2008). Because CT-like cross-sectional brain
images are also provided within the angiosuite, procedural complications such as intracranial hemorrhage
may be recognized early and without the need for
patient transfer.
CBA
Valdueza et al., Neurosonology and Neuroimaging of Stroke: A Comprehensive Reference, Second Edition (ISBN 978-3-13-141872-2), copyright © 2017 Thieme Medical Publishers
All rights reserved. Usage subject to terms and conditions of license.
Fig. A6.2 Right frontobasal AVM, visualized by using conventional lateral projection image (A), 3D rotational angiogram (B) and
3D top-down view (C), superimposed on the DynaCT cross-sectional image for neurosurgical planning.
185Digital Subtraction Angiography (DSA)
Tec hnic al A spects o f Me chan ical Thr ombec tomy
There are diff erent ways of dissolving a thrombotic in-
tracranial vessel occlusion, which may be subdivided into
intravenous and intra-arterial pharmacological clot lysis
as well as mechanical thrombectomy.
Since the results of the National Institute of Neurological Disorders and Stroke t-PA study, followed by its U.S.
Food and Drug Administration (FDA) approval in 1996,
intravenous thrombolysis has remained the mainstay
of stroke treatment for almost two decades. Yet, it has
become obvious that certain clot types (defi ned by clot
burden, site of vessel occlusion, clot consistency, clot age,
etc.) are less prone to intravenous lysis and consequently
associated with worse clinical outcome. Occlusion of major vessels such as the M1-middle cerebral artery (MCA)
segment as well as carotid and basilar artery occlusions
have been recognized as critical sites, requiring additional approaches such as intra-arterial lysis with or without
mechanical clot disruption using a microwire or microcatheter.
Even then, a signifi cant number of clots could not be
dissolved, triggering the development of other mechanical thrombectomy devices, of which the fi rst-generation
retrieval system MERCI, as well as the second-generation
stent retrievers TREVO and SOLITAIRE, have gained FDA
approval. TREVO and SOLITAIRE have proved superior
to the MERCI retrieval system in recent studies (SWIFT,
TREVO-2) (Nogueira et al 2012, Sheth et al 2015). In February 2015, results of the fi rst randomized clinical trial
showing effi cacy and safety of mechanical thrombectomy
as compared with intravenous lysis solely in the proximal anterior circulation were published, representing a
breakthrough for endovascular stroke treatment (Berkhemer et al 2015). Soon after that, various other studies
(ESCAPE, SWIFT PRIME, EXTEND-IA) were halted because
interim analysis signifi cantly favored endovascular stroke
treatment by thrombectomy (Campbell et al 2015, Goyal
et al 2015, Saver et al 2015).
Apart from clot manipulation by retrieval systems, suction thrombectomy (also called the direct aspiration fi rst
pass technique [ADAPT], with or without the use of an
external pump system, has regained attention. Improved
catheter technologies make it possible to place large-bore
catheters at or right in front of the occlusion site, with
average recanalization times of ~30 minutes (Park 2015)
or even less. At present, a sequential approach using the
ADAPT technique, followed by stent retriever thrombectomy if ADAPT fails, seems to be the most promising and
cost-eff ective procedure (Turk et al 2014).
A common technical protocol for M1-MCA recanalization includes placement of a long sheath (6–8 Fr, for the
best possible stability in often elongated access vessels)
with the tip in the cervical internal carotid artery (ICA) segment, coaxial advancement of a large-bore suction catheter (e.g., 5MAX ACE, Penumbra Inc.), via a microcatheter
to the occlusion site and either penetrating the thrombus
slightly with the suction catheter or starting suction right
in front of the clot. After a short time (usually 3–5 minutes)
the suction catheter is removed under continuous suction
at the catheter orifi ce as well as the sheath sidearm. Fol-
lowing removal, the catheter and aspiration pump (if used)
are checked for thrombus material. If recanalization is
not achieved, the procedure can be repeated (usually 1–2
times), before a stent retriever is unboxed and introduced
via the micro- and guide catheter in a coaxial manner.
After the stent is placed within the thrombus by retracting the microcatheter, fl ow is usually already restored to
some extent. For optimal thrombus penetration the stent
retriever is left in place for 2–5 minutes and is then withdrawn into the guide catheter during suction. Again, this
procedure may be repeated 1–2 times if required. A more
detailed overview of the mechanical techniques used in
acute stroke is given in the literature (Spiotta et al 2015)
(Fig. A6.3, Fig. A6.4).
Advantages and Disadvantages
DSA is considered to be the gold standard whenever the
best possible detail resolution and/or assessment of cerebral hemodynamics are required.
Despite being regarded as state-of-the art, the spatial
resolution of fl at-panel DSA still does not compete with
fl at-panel volume CT systems. The latter are based on a CT
gantry, yielding spatial resolutions as low as 150–200 mm.
Flat-panel DSA is restricted to inferior spatial resolution
because of geometric inaccuracies, blurring due to the
X-ray converter and reconstru ction fi lter, and dose consid-
erations. A CT slip-ring technique is not available for 3D
186 6 Angiographic Techniques in Neuroradiology
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CDBA
Fig. A6.3 77-year-old woman presenting with right-sided hemiplegia and global aphasia. Onset was determined as 4 hours before imaging. (A) Noncontrast CT, axial plane, on admission. No early signs of ischemic stroke are depicted. (B,C) CT perfusion maps, showing
extended hypoperfusion in the left MCA territory (B, time-to-drain map), with only slight reduction in cerebral blood volume, indicative of
a signifi cant penumbra. (D) CTA, frontal volume-rendered reconstruction. A proximal M1 occlusion is visualized (arrow).
AB CD
Fig. A6.4 DSA, frontal view, before (A) and after (B) suction thrombectomy, using the ADAPT technique. The large-bore aspiration catheter
(5MAX ACE Reperfusion Catheter) was advanced to the proximal thrombus end (arrow) and the aspiration pump turned on for ~5 minutes.
After catheter retraction, thrombotic material was found within the reperfusion catheter as well as within the syringe, used for supportive suction at the sheath sidearm during the retraction procedure. The control run (B) shows complete MCA revascularization (TICI 3).
Follow-up brain MRI on day 1, following ADAPT thrombectomy. (C) Axial DWI image (b = 1,000), showing only small and scattered, hyperintense ischemic lesions within the left-sided MCA territory. (D) 3D TOF-MRA, showing persistent recanalization of the left M1-MCA and
adjacent vessels.
rotational angiography, thus disabling continuous C-arm
rotation for time-resolved imaging in fl at-panel volume CT.
As described previously, vascular imaging issues are
constantly changing and cerebrovascular hemodynamics may now be assessed noninvasively by time-resolved
MRA or CTA techniques. Still, none of these alternative
four-dimensional (4D) techniques can provide spatial
and temporal resolution comparable to DSA, as might be
required in the assessment of complex AVMs. If interventional procedures are necessary within a short period of
time, such as in patients with intracranial major artery
occlusion, invasive catheter angiography remains the
fi rst-line diagnostic and therapeutic modality.
Contraindications to DSA are comparable to CTA as
they are generally related to the use of iodinated contrast
medium as well as ionizing radiation. Renal insuffi cien-
cy, hyperthyroidism, and iodine allergy are common although not absolute contraindications to DSA (as well as
CTA). Pregnancy is also a contraindication for DSA unless
the angiography is of vital importance for the mother.
Procedural complications have been reported to
amount to a 1–2.3% overall incidence of neurologic defi cit
and a 0.4–0.5% incidence of persistent defi cits following
cerebral angiography (Heiserman et al 1994, Leff ers and
Wagner 2 000) . However, non -neurologic complications
such as local hematomas were observed in 14.7% of procedures in the Leff ers and Wagner study. Clinically silent
embolisms were encountered in up to 44% of patients
undergoing DSA, if suff ering from vascular risk factors
(Bendszus et al 1999). These fi gures might seem signif-
icant, but in the Leff ers and Wagner study, the majority
of non-neurologic complications were minor groin hematomas. In addition, Burger et al (2006) showed in a study
of DSA-related complications in pediatric neuroangiography, which is technically more demanding than in adults,
that in experienced hands this is a low-risk procedure
(they reported no intraprocedural complications in 241
consecutive pediatric cerebral angiograms). Also other
studies have proven DSA to be a safe procedure, especially if performed in centers that carry out large numbers of
procedures (Fifi et al 2009, Thiex et al 2010).
Radiation exposure is a variable that depends on various factors, such as the DSA procedure itself (diagnostic
or interventional), number of vessels assessed, vascular
anatomy (elongation, anatomic variants), operator experience, and the angiography suite used (biplane, 3D rotational, or fl at panel). Diff erent exposure parameters are
in use, such as eff ective dose (ED), CTDI, or organ dose
(e.g., lens dose). A typical four-vessel angiogram was
found to result in a patient ED of 3.6 millisievert (mSv)
187Magnetic Resonance Angiography (MRA)
Valdueza et al., Neurosonology and Neuroimaging of Stroke: A Comprehensive Reference, Second Edition (ISBN 978-3-13-141872-2), copyright © 2017 Thieme Medical Publishers
All rights reserved. Usage subject to terms and conditions of license.
(Marshall et al 1995) which is within the range for multislice cervicocranial (cc) CTA using older-generation MSCT
scanners (for 4- and 64-slice CTA).
When compared with biplane DSA, rotational 3D
DSA resulted in signifi cantly lower skin doses; up to four
times lower peak skin doses were reported by Schueler
et al (2005). ED measurements in fl at-panel rotational
DSA and multislice CT showed identical dose fi gures for
3D angiography as compared with biplane (2D) DSA, and
comparable ED fi gure ranges for multislice and fl at-panel
cranial CT (Struff ert et al 2014). The dose received during
CTA has also been described as equivalent to ~15 minutes
of fl uoroscopy time, e.g., somewhat greater than typical-
ly required for routine diagnostic DSA but not outside
the safe limits for diagnostic radiologic assessments
(Chappell et al 2003).
DSA may also be performed by intravenous injection
and this technique was fi rst developed in the late 1970s.
This type of DSA compares an X-ray image of a region of
the body before and after a radio-opaque iodine-based dye
has been injected intravenously into the body. Tissues and
blood vessels on the fi rst image are digitally subtracted
from the second image, leaving a picture of the artery of
interest. Despite its obvious advantages compared with the
intra-arterial catheter technique it has not gained much
signifi cance mainly because of its inferior resolution com-
pared with conventional DSA and the advantages of MRA,
CTA, and duplex sonography as alternative noninvasive
procedures. Recently, however, a DSA technique with intravenous contrast medium injection has been proposed,
using a biplane fl at-detector angiographic system; this
technique provided high-resolution assessment of the
intracranial vasculature in general (Saake et al 2013) and
also showed promising results in evaluating aneurysm
remnants after neurosurgical clipping (Gölitz et al 2012).
Magnetic Resonance Angiography (MRA)
Historical Development
Nuclear magnetic resonance (NMR) imaging, the original
term for MRI, designates a radiation-free imaging technique based on the proton nucleus resonance in response
to a radio-frequency pulse, emitted and received by
so-called “coils” within a dedicated scanner. The basic
physical principle was described by Bloch and Purcell in
1946, but it was Paul Lauterbur and Peter Mansfi eld (the
two shared the Nobel Prize in 2003 for their MRI achievements) who in the early 1980s developed the underlying
principle into a technique that allowed the generation
of images of the human body (Andrew 1992). For image
generation and spatial encoding, magnetic gradients are
applied together with the radio-frequency pulse. The
resulting data are recorded in a 2D or 3D image matrix and the image itself then is created by applying an
a l g o r i t h m c a l l e d F o u r i e r t r a n s f o r m a t i o n . B y v a r i a t i o n o f
scanning parameters, tissue contrast can be altered and
enhanced in various ways to assess diff erent properties.
In MR angiography (MRA) the introduction of FLASH
sequences (Fast Low Angle Shot) in 1985 by Frahm
et al (1986) allowed signifi cant shortening of MRI
m e a s u r e m e n t t i m e s , b y c o m b i n i n g a g r a d i e n t e c h o
sequence (using a low-fl ip angle pulse) with a rapid
sequence repetition. In 1996 time-resolved ce 3D MR angiography (also called 4D-MRA) was introduced (Korosec
et al 1996), with ce 4D MRA now being a widely used
noninvasive dynamic angiography technique.
In recent years advances in scanner and software
technology, as well as health-care reimbursement issues,
have shifted boundaries in regard to selecting the most
cost-eff ective procedure.
Technical Aspects
MRA is a widely used noninvasive imaging tool for the
cervicocranial vasculature that involves no radiation exposure. MRA is based on intrinsic or extrinsic vessel contrast. Various ce and non-ce MRA techniques have been
established, requiring some background knowledge to
tailor the MR study design to a particular clinical question. In addition to primarily angiographic MR data acquisition, the postprocessing of ce volume data, such as with
3D magnetization-prepared rapid acquisition with gradient echo (MPRAGE), yields near-angiographic images
(Fig. A6.5). Although these maximum intensity projected
images do not provide detailed vessel assessment, they
may nevertheless aid in extracting vascular pathology
from routine scans.
The primary vascular imaging techniques with
intrinsic contrast are time-of-fl ight (TOF) MRA (Fig. A6.6)
and phase-contrast (PC) MRA (Fig. A6.7). Other recently evolved and refi ned techniques that do not require
intravenous application of contrast media include electrocardiograph (ECG)-gated fast spin echo (FSE), steadystate free precession (SSFP), and arterial spin labeling
(Miyazaki and Lee 2008, Morita et al 2011). ECG-gated
FSE angiography is predominantly used for assessing
peripheral arteries based on its sensitivity to slow fl ow,
whereas SSFP with ECG gating is applied to aortic and
coronary artery imaging (Morita et al 2011). Arterial
spin labeling uses blood as an endogenous contrast agent
BA
Fig. A6.5 Coronal MIP reconstructions from contrast-enhanced
3D MPRAGE, providing approximate angiographic information.
(A) Intracranial main-stem arteries as well as the bilateral elongated
sub-basal ICA courses are depicted. (B) A developmental venous
anomaly is shown (thick arrow), accompanied by a prominent
draining vein (thin arrows).
188 6 Angiographic Techniques in Neuroradiology
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All rights reserved. Usage subject to terms and conditions of license.
A
B
Fig. A6.6 3D TOF-MRA using a current 3-T scanner. The axial
(A) and coronal (B) MIP view show excellent detail resolution, permitting assessment of even peripheral branches (e.g., of the M3
segments of the MCA).
BA
commonly implemented with partial-Fourier FSE and
balanced SSFP techniques (Miyazaki and Lee 2008).
In this context, the technique of black-blood imaging
has to be mentioned, despite the fact that it does not deliver any angiographic images; this technique can be used
to evaluate vessel wall pathology as it suppresses signals
from fl owing blood by using an FSE sequence with double
inversion recovery and ECG gating. As ischemic events can
be triggered by so-called vulnerable plaques, e.g., plaques
with a necrotic core, intraplaque hemorrhage, and a thin
fi brous cap (Gupta et al 2013), the potential of black-blood
imaging in diff erentiating a recent hemorrhage from a
lipid-rich necrotic core seems valuable (Morita et al 2011).
The use of intravenous contrast medium (gadolinium) is
required in dynamic MRA as well as in the 3D GE FLASH
technique (Fig. A6.8B and Fig. A6.9B).
Time-of-fl ight (TOF) MRA
Worldw ide, TOF-MR A is the M RA t echnique mo st comm only used for intracranial vessel assessment. The name refers to
the limited time (the time of fl ight) during which infl owing
protons provide high signal intensity, whereas stationary
proton signals are eliminated by repeated saturation pulses. Most commonly, a gradient echo measurement is performed, characterized by short signal repetition time (TR)
and slice acquisition perpendicular to the direction of blood
fl ow. The diff erence between the unsaturated and presatu-
rated spins leads to high intravascular signal intensity. The
fl owing blood moves unsaturated spins from outside into
the imaging plane and enables signal generation, as opposed to the stationary and saturated tissue spins. When a
presaturation slab is established on one side of the imaging
plane, those spins that fl ow in from the same side also do
not deliver a signal, thus rendering this technique direction
sensitive for either arteriography or venography. Only fresh
infl owing blood will deliver the maximum signal; therefore,
slow or turbulent fl ow, inappropriate slice thickness, and/or
inadequate TR all have an impact on signal characteristics
and thus may mimic or mask vascular pathology. Various
means to improve the vascular signal intensity have been
introduced such as multiple overlapping thin slab acquisition (MOTSA) and tilt optimized nonsaturated excitation
(TONE) techniques, both of which focus on minimizing partial saturation eff ects of infl owing protons.
Phase-contrast (PC) MRA
Phase shifting of fl owing protons as well as blood fl ow
Fig. A6.7 Phase-contrast MR angiography. Although there is
a r t e r i a l a s w e l l a s v e n o u s v e s s e l c o n t r a s t , t h e c l i n i c a l p e r t i n e n t i n formation in regard to presumptive sinus venous thrombosis on
the coronal (A) and sagittal (B) plane is readily available, ruling out
cerebral venous thrombosis.
by magnetically labeling it with radio-frequency pulses
and has shown promising results with respect to brain
perfusion assessment in various cerebrovascular disorders, including acute stroke (Bokkers et al 2012, Deibler
et al 2008). It may also be used for morphological vessel
evaluation, e.g., of the abdominal and cervical arteries,
velocity are the decisive factors of the PC technique. PC
angiography requires data acquisition with and without
fl ow encoding in three diff erent planes, with subsequent
image subtraction. Thus complete background suppression is achieved, superior to TOF-MRA. Yet, acquisition
time is increased as compared with TOF-MRA, because
fl ow encoding can only be done along one axis at a time.
Attention has to be paid to the velocity encoding (VENC)
gradient, as a VENC mismatch to the true velocity might
lead to image artifacts that may mimic stenosis. 2D as
well as 3D PC sequences are currently employed, the fi rst
being used for vessel “scout scans,” cine imaging, fl ow
quantifi cation, or thick slab imaging of the dural sinus.
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